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Pitch-Synchronous Changes in the Anterior Cricothyroid Space During Singing
Journal of Voice Vol. 16, No. 2, pp. 182–194 © 2002 The Voice Foundation
Pitch-Synchronous Changes in the Anterior Cricothyroid Space During Singing *Anne-Maria Laukkanen, †Raija Takalo, ‡Miika Arvonen, and ‡§Erkki Vilkman *Department of Speech Communication and Voice Research, University of Tampere, Tampere, Finland; †Departments of Diagnostic Radiology and ‡Otolaryngology and Phoniatrics, University of Oulu, Oulu, Finland; §Helsinki University Central Hospital, Helsinki, Finland
Summary: Pitch-synchronous changes in the anterior cricothyroid (CT) space were registered with ultrasonography (USG) for ten healthy subjects (5 males, 5 females) during the production of musical fifths throughout the whole voice range. One of the males and one of the females were trained amateur singers, the other subjects were choir singers. The average decrease in CT space per a musical fifth was 1.3–2.4 mm for the males and 1.0–1.8 mm for the females; the average decrease was smaller in the middle of the pitch range for both genders. The results suggest that (1) USG can be used for detection of pitch-synchronous changes in the CT space; (2) these changes are dependent on pitch range; and (3) more trained singers tend to have somewhat smaller changes than less trained subjects at certain frequencies. The results seem to indicate that F0 control mechanism varies according to pitch range and register, and possibly according to individual structure and vocal technique related differences. Key Words: Ultrasonography—F0 control—Singing—Register.
roarytenoid muscle (TA)10–12 and subglottic pressure in F0 control has also been studied.12–13 Contraction of TA has been found to be related either to a decrease or to an increase in F0.13–15 It has been stated that the role of TA in F0 control depends on the activity relation between TA and CT15 and on the amplitude of vibration of the vocal folds.12 Contraction of TA increases the stiffness of the muscular layer of the vocal fold. Thus, increased activity of TA raises F0 if the activity of the CT is not near its maximum and when the amplitude is large enough to involve the muscular layer of the vocal fold. This holds true for phonation at lower pitches and when the intensity of phonation is sufficiently great. When the amplitude of vibration of the vocal folds is low and the vibration concentrates mainly on the cover part, contraction of TA lowers F0, since it loosens the cover. Increased activity of the TA muscle thus tends to
INTRODUCTION Fundamental frequency (F0) can be varied by changing the vibrating mass and/or the stiffness of the vocal folds.1–3 The relationship between mass and F0 is inverse while the relationship between stiffness and F0 is direct. Stiffness can mainly be increased and the effective mass decreased by the cricothyroid (CT) muscle, which elongates the vocal folds by approximating the cricoid arch and the thyroid cartilage.4–5 There is evidence that the vocal folds lengthen as F0 is raised.1,6–9 The role of the thyAccepted for publication August 20, 2000. Address correspondence and reprint requests to Anne-Maria Laukkanen, PhD, Department of Speech Communication and Voice Research, University of Tampere, FIN-33014 Tampere, Finland. e-mail: [email protected]
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CRICOTHYROID SPACE lower F0 at high frequencies and when intensity is low. An increase in subglottic pressure may raise F0 by increasing the amplitude of vibration of the vocal folds, which in turn, increases the stiffness of the vocal fold cover.16 It has been suggested that different mechanisms may be applied at different pitch ranges11 and in different registers8,17–19 and that there may also be individual differences in the use of F0 control mechanisms.8 F0 control has mainly been studied by using x-ray and electromyographic (EMG) methods. Both methods are invasive and even risky. Noninvasive methods can also be used to some extent. For example, F0 control through activation of the cricothyroid muscle should be indicated in changes of the CT space. Those, in turn, should be seen by using ultrasound (US) examination. Vilkman et al20 studied the physiological background of sentence declination and stress production using US method. The results suggest that the method is usable for studying F0 control mechanisms. The purpose of the present study was to investigate changes in the anterior cricothyroid space as a function of changes in F0 during singing. The US method was applied. MATERIALS AND METHODS Subjects and the task Ten healthy subjects (5 males, 5 females, mean age 29.4 years, range 21–44 years) volunteered as subjects for the study. One of the males (subject E) and one of the females (subject J) were trained amateur singers with approximately 10 years and 5 years of study in classical singing. The other subjects were choir singers with an average of 8 years (range 3–19.5 years) experience but without any formal singing training, except for one, subject G, who had been studying singing for 6 years. Since, however, her singing style in these experiments did not differ from that of the other choir singers, she will be classified as an untrained choir singer in this study. The perceptual differences between the singing styles used by the choir singers and the trained singers were a more falsettolike voice quality with less marked vibrato in the choir singers, while the trained singers used a more “mixed register” type of voice quality and had a clear vibrato in their samples. The subjects sang musical fifths up and back downward (e.g. C-G-
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C) on vowel [!:] throughout their vocal range starting from the lowest sustainable tone and continuing up to the highest one. In order to keep the test duration reasonable, only those fifths were included whose starting pitches are in C major. The duration of each note sung was approximately two seconds. The task was completed twice. The subjects were lying supine during the test, which was necessary for the US registration. Ultrasonography The US examination was accomplished at the Department of Diagnostic Radiology at Oulu University Hospital by an experienced radiologist (one of the authors, RT). In the examination a real-time scanner (GE Logiq 500MD) and a 13-MHz linear transducer were used. This US transducer type has a high resolution for objects near the surface. The transducer was placed tightly against the skin anteriorly on the larynx in the midline. Figure 1 illustrates the examination procedure. The US images and the audiosignal were stored on videotape. The frame interval of the videorecorder was 40 ms. The CT space was measured in the middle of each note. The echoes caused by the calcified areas close to the anteroinferior edge of the thyroid cartilage and the anterosuperior edge of the cricoid cartilage were used as points of measurement (see Figure 2). The measurements were performed manually on a monitor screen with the aid of a pair of dividers. The monitor offered a quadruple magnification, which increases the accuracy of the measurement. The values were calibrated against the recorded scales available in the US device. For each musical fifth the optimal points of measurement, i.e., calcified areas with clearly discernible contures, were chosen. It should be noted that these points were not necessarily located exactly at the border of the cartilages. Hence the CT distance obtained does not represent the true CT space. Moreover, as the projection changes due to changes in the laryngeal position during the production of a wide pitch range, the contures of the calcified areas on the USG display change accordingly. For these reasons only changes in the CT distance for a given musical fifth can be studied using the US method. The measurements were made by an experienced radiologist (author RT). Some of the samples were Journal of Voice, Vol. 16, No. 2, 2002
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FIGURE 1. Ultrasound examination procedure.
also measured by another experimenter (author MA) to obtain interrater correlation. Frame was standardized in the measurements. The results from repeated measurements accomplished by the same examiner on two successive days did not differ significantly from each other (Student’s t test; t = 0.00, d.f. = 35, S = 1.000) and there was a perfect correlation between them (r = 1.00; P = 0.000). The results obtained by the two examiners also correlated strongly with each other (r = 0.96; P = 0.000). Figure 3 shows the correlograms. In the repeated measurements made by the same examiner the results matched perfectly in 77.7% of the cases and in 22.2% of the cases the results were within ±0.03 cm. The two examiners agreed perfectly in 11.1% of the cases, and in 55.5% of the cases the difference between their results was within ±0.03 cm. It is concluded that the measurement accuracy was sufficient.
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FIGURE 2. Longitudinal ultrasonographic scan of the anterior cricothyroid space. T = thyroid cartilage, C = cricoid cartilage. CT space measured as the distance between the points marked with an asterisk (*).
RESULTS Figures 4 and 5 show the average pitch-synchronous changes in the CT space during the production of the musical fifths both upward and downward. A comparison between trained singers and choir singers is seen in Figure 6. The pitch-synchronous changes in the CT space are given for each subject separately in the Appendix. As can be expected, CT space diminished in most cases as pitch rose, only a few exceptions were observed (see Figure 6B and Appendix). The average change in CT space per one ascending musical fifth was -0.17 cm for the males (SD = 0.12 cm) and -0.14 cm for the females (SD = 0.09 cm). Figure 4 suggests that there was a tendency for the change in CT space to be smaller in descending fifths. In Figure 5 it can be seen that this tendency was mainly true for the fe-
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A
B
FIGURE 3. Correlograms for (A) repeated measurements made by the same examiner, and for (B) measurements accomplished by two examiners.
males, while for the males the average change in CT space was in most cases larger in descending fifths. The average change in CT space was for the males the same in descending musical fifths as in ascending fifths (mean-0.17 cm, SD = 0.12 cm). For the females the average change was slightly smaller in descending fifths (mean change-0.12 cm, SD = 0.10 cm). The average difference between CT space changes in ascending and descending fifths (calculated in absolute values of the CT space change) was 0.04 cm for the females (28%) and 0.03 cm for the males (18%). The difference between the genders was nonsignificant in pitch change upward but sig-
nificant in pitch change downward (Mann-Whitney U test, U value = 63.5, ␣ = 0.01). As can be seen in Figures 4–6, the changes in CT space occurred nonlinearly and were smaller and larger at certain pitch areas. In general, smaller changes were seen in the middle of the pitch range (located mainly in the third octave for the males and in the fourth for the females) than at lower and at higher pitches (in the second and the fourth octaves for the males and in the third and the fifth octaves for the females). In the highest musical fifths the changes in CT space were, in general, small. The average change in ascending fifths at the lowest pitch-
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FIGURE 4. Average pitch-synchronous changes of the cricothyroid (CT) space (in centimeters, vertical axis) for ten subjects singing musical fifths upward and downward. A negative value shows a decrease in CT space as pitch rises. The change in CT space was positive in descending fifths but the changes are given in negative values in order to make a comparison between ascending and descending fifths easier. Numbers on the horizontal axis refer to musical fifths, 1 being the lowest produced by each subject. Number of subjects per each musical fifth: 10 for 1st–8th, 9 for 9th, 8 for 10th, 7 for 11th and 12th, 6 for 13th, 5 for 14th, 4 for 15th, 3 for 16th, and 1 for 17th.
es was -0.26 cm (SD = 0.15 cm) for the males and -0.17 cm (SD = 0.08 cm) for the females. At the middle of the pitch range the average change in CT space was -0.12 cm (SD = 0.07 cm) for the males and -0.08 cm (SD = 0.06 cm ) for the females. At the higher pitches (the highest excluded) the average change was -0.24 cm (SD = 0.08 cm) for the males and -0.17 cm (SD = 0.11 cm) for the females. The differences between the lowest and the middle pitch ranges were nonsignificant for both genders, while the middle and the highest pitch ranges differed significantly from each other (Mann-Whitney U test, for the males U value = 55.5, ␣ = 0.001, for the females U value = 63.5, ␣ = 0.001). The female choir singer, subject G, who had received singing training made an exception to the general pattern (see Appendix): For her the changes in CT space became fairly linearly smaller as pitch increased. The trained subjects (subjects E and J) showed in the middle of the range smaller changes in the CT space than the choir singers, while at the lower pitch range the largest change was seen for subject E (Figure 6). The average pitch increase related decrease in the CT space was smallest at the 3rd–4th musical fifth Journal of Voice, Vol. 16, No. 2, 2002
and at the 6th–9th musical fifth (Figure 4). For individual subjects, then, either the starting note or the ending note of these musical fifths was located at C3F#3 and D4-F#4 in the males and at D4-F#4 and C5E5 for the females (see Table 1). These pitch ranges are known as register transition areas. According to the authors’ perception the voice quality of most of the subjects changed more or less clearly toward a falsetto quality especially at the higher transition area. Friedrich and Lichtenegger21 made morphological measurements on 50 human laryngeal preparates to determine the average configurations and dimensions of cartilages and soft tissues of the larynx. Based on these measurements it can be estimated that for the males a 1-mm decrease in the CT space would bring about an increase of 1.4 mm in the length of the membraneous portion of the vocal folds, while for the females only a 0.5 mm change in length would take place. Considerable individual differences are expected, since location of the rotation center point between cricoid and thyroid cartilages naturally varies due to differences in the laryngeal geometry. Additionally, these estimations do not take into ac-
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A
B
FIGURE 5. Average pitch-synchronous change of cricothyroid (CT) space (in centimeters, vertical axis) for (A) 5 females and (B) 5 males singing musical fifths upward and downward. The change in CT space was positive in descending fifths but the changes are given in negative values in order to make a comparison between ascending and descending fifths easier. Horizontal axis: number of musical fifths, 1 being the lowest produced by each subject. Number of female subjects per musical fifths: 5 for fifths 1–9, 4 for 10–12, 3 for 13–16, and 1 for 17. Number of male subjects: 5 for fifths 1–8, 4 for 9–10, 3 for 11–13, 2 for 14, and 1 for 15.
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A
B
FIGURE 6. Average change of cricothyroid (CT) space (in centimeters, vertical axis) for one trained and four untrained females (A) and for one trained and four untrained males (B) singing musical fifths upward. Horizontal axis: number of musical fifths (1 is the lowest).
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TABLE 1. Musical Fifths with Smaller than Average PitchSynchronous Changes in the CT Space Males Subject A Subject B Subject C Subject D Subject E (trained)
A2 - E3 B2 - F3 B2 - F3 F2 - C3 A2 - E3
C3 - G3 E3 - B3 E3 - B3 C3 - G3 D3 - A3
E3 - B3 G3 - D4
Females Subject F Subject G Subject H Subject I Subject J (trained)
G3 - D4 A3 - E4 A3 - E4 A3 - E4 A3 - E4
D4 - A4 E4 - B4 E4 - B4 D4 - A4 D4 - A4
G4 - D5 A4 - E5
count the possible effect of cartilage gliding on vocal fold length. Furthermore, the effect of a change in vocal fold length on F0 is dependent on the actual stiffness of the vocal folds and subglottic pressure.12,22 Therefore only a rough estimation can be given for the relationship between a change in CT space and a change in vocal fold length. In the present study the average change in CT space per one ascending musical fifth was 1.7 mm for the males and 1.4 mm for the females. According to the estimation these changes would correspond to changes of 2.4 and 0.7 mm, respectively, in the length of the membraneous portion of the vocal folds. This, in turn, would make a change of 0.34 mm per semitone in the length of the vocal folds for the males and a change of 0.1 mm per semitone for the females. In Figure 7 changes in the CT space for subject F (female) have been translated into changes in vocal fold length and compared with the x-ray results obtained by Sonninen et al9 for pitch-synchronous changes in the distance between the anterior ossification centers of the thyroid (T) and the arytenoid (A) cartilages for one trained soprano singing in forte covered mode. This T-A distance gives approximate information of vocal fold length. Data of the present study and those of Sonninen et al bear resemblance: Pitch-synchronous changes in both the CT space and in the T-A distance were smaller in the middle of the pitch range and various dips occurred in both curves at register transition areas.
B3 - F4
G3 - D4
A4 - E5 E4 - B4
DISCUSSION Kitajima and collaborators reported that a decrease of 1 mm in the CT space of human larynx preparates (male and female larynges) brought about an increase of 0.15–0.90 semitones in pitch.23 In the present study much smaller pitch-synchronous changes in CT space were found. This discrepancy is most likely due to the higher stiffness of the vocal folds in living subjects. According to the x-ray study of Sonninen et al for 10 trained singers, the pitch-synhronous changes in the length of the vocal folds varied between 2–9.5 mm.1 When a correction for projection error is made the values are within 1.6–7.45 mm. On the basis of these values, and the pitch range sung by the subjects in Sonninen’s study, it is possible to calculate a mean change of 0.10–0.23 mm per semitone for the females and a mean change of 0.08–0.17 mm per semitone for the males. The changes observed by Nishizawa et al with stereoendoscopy were 0.7–3.5 mm per octave for the males and 1.5–2.1 mm per octave for the females (untrained singers).8 This makes a change of 0.12–0.17 mm per semitone for the females and a change of 0.06–0.29 mm per semitone for the males. The values obtained in the present study as the changes in CT space were translated into changes in vocal fold length and are reasonably within those reported by Sonninen and by Nishizawa et al. This suggests that the measurement accuracy of the US method was sufficient and that the subjects Journal of Voice, Vol. 16, No. 2, 2002
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FIGURE 7. Comparison between x-ray data on pitch-synchronous changes in thyroarytenoid distance (corresponding to vocal fold length) for one trained female soprano singing in forte covered mode and USG data on changes in cricothyroid (CT) space for one untrained female (subject F) singing musical fifths upward. Changes in CT space have been translated into changes in vocal fold length based on the measurements of Friedrich and Lichtenegger (1997). Vertical scale is in millimeters. Numbers on the horizontal axis refer to musical fifths, 1 being the lowest produced by each subject. The x-ray data were obtained from a study by Sonninen et al (1999).
accomplished F0 control mainly by rotation of the cricothyroid articulation. The average value for the males is made higher by the values of subject D. His values may be higher because he was the oldest of the choir singers (44 years) and he also had the lowest pitch range. According to the results obtained in the present study, pitch-related changes in CT space seemed to be pitch dependent. The results appear logical. In the very lowest musical fifth the pitch-synchronous decrease in CT space was smaller than that in the next musical fifth starting one tone higher. This may indicate that the role of thyroarytenoid muscle, and possibly also that of subglottic pressure in F0 regulation, is at the lowest pitch range larger than at higher pitches where F0 is mainly regulated by cricothyroid muscle. Atkinson reported (for one male subject, though) that at the lowest pitches F0 is raised through the activation of the vocalis muscle and at higher pitches the task is accomplished with the cricothyroid muscle.11 Isshiki, in turn, suggested that in falsetto register F0 is mainly regulated by subglottic pressure.18 At the very lowest pitches voice production is mainly falsettolike (characterized by incomplete glottal closure).24 The fact that smaller changes in CT space were seen in the middle pitch range might indicate deJournal of Voice, Vol. 16, No. 2, 2002
creased activity of the vocalis related to a shift from a heavier register to a lighter one (from “modal” to “middle register” or to “falsetto”). As the activity of the vocalis decreases, the vocal fold cover gets stiffer and a smaller increase in vocal fold length is needed to increase vocal fold stiffness further. This can also explain the fact that fairly small changes in CT space were seen in the highest pitches of each subject’s range. Furthermore, the changes in CT space seemed to be smallest in those musical fifths in which either the lowest or the highest tone was located at register transition areas. In the perception of the authors, the subjects also tended to decrease the intensity in those tones. In general, the results of the present study, as well as those obtained by Sonninen et al9 seem to indicate that there are various biomechanical areas or registers in human pitch range. The result that the pitch-synchronous change in CT space increased again at pitches above the middle range are also in line with the observations of Sonninen et al on changes in the T-A distance (i.e., length of the vocal folds) (see Figure 7). This might be explained as follows. The activity of both CT and TA has been found to increase simultaneously as pitch is raised.22 It is possible that at the highest pitches in a register (i.e., at pitches somewhat below a register transition) the
CRICOTHYROID SPACE activity of TA gets so strong compared to that of CT that a greater stretch of the vocal fold is needed to raise pitch further. The trained subjects showed slightly smaller changes in CT space in the middle range; this seems to suggest that trained subjects relax the vocalis more. These results are in accordance with those obtained by Sonninen et al.9,25 In trained singers and in one trained soprano singing in the “covered” mode, i.e., the typical voice production of trained singers, the pitch-synchronous increase in vocal fold length was smaller than in untrained singers and in the trained soprano’s open mode of singing, which corresponds to an untrained singer’s speechlike singing. On the other hand, the trained male singer of the present study (subject E) had a large change in CT space at the low-pitch range. This, in turn, might be explained by a strong vocalis activity. It seems plausible that at the low-pitch range this singer sang louder and with fuller modal register quality than the untrained singers. The authors’ perceptual observations support this suggestion. The female choir singer (subject G) with singing training showed the smallest CT space changes in the highest pitch range. This may reflect individual structural and/or behavioral differences. It may show that she was skilled in relaxing vocalis activity with pitch rise or that she used the purest falsetto type of voice. The observation may also be related to the fact that she had the highest soprano voice among the subjects. The change in CT space was in some cases—especially for the females—somewhat smaller during pitch change downward than when pitch was raised. For the males the change was in most cases larger in descending fifths. These findings could reflect changes in voice intensity. When intensity is lowered together with pitch, somewhat longer and thus stiffer vocal folds are needed to avoid excessive pitch drop.22 On contrast, if intensity is higher at the lowest notes of the fifths the CT space must be opened to reach as low a pitch as needed. The smaller change in CT space during pitch lowering could also be explained by the so-called hysteresis effect.26 During longitudinal stretch, a tissue, e.g., vocal fold, loses its stiffness to a certain degree. Therefore the same fundamental frequency (F0) can be obtained with longer vocal folds when pitch is shifted downward. This phenomenon seemed to be stronger in the females. This, as well as the fact that slightly smaller changes
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in CT space were measured for the females than for the males, could be explained by suggesting that the female vocal fold tissue is somewhat stiffer than that of the males. There is some evidence supporting this supposition. Various authors have come to the conclusion that differences in F0 between the sexes cannot be explained merely through differences in the laryngeal size.27,28 Nishizawa et al reported (for untrained singers) smaller pitch-synhronous changes in the vocal fold length for the females than for the males.8 Furthermore, according to the results of Müller obtained from human larynx preparates, the maximum stretch-induced change in vocal fold length was 5 mm for the males and 3 mm for the females.29 On the other hand, Sonninen and Hurme observed (for trained singers) larger pitch-synhronous length changes in the vocal folds of their female subjects compared to the male subjects.25 This discrepancy might be explained by differences in the individual and in vocal technique. A supine position may have some effect on voice production. As the direction of gravitational force changes, it alters the biomechanical conditions for the respiratory and laryngeal muscles (about respiration see, for example, Hixon and collaborators30 and Sundberg et al31; about external laryngeal frame function see Sonninen1 and Vilkman et al32). Furthermore, to obtain a clear image and to avoid projection errors, the US probe has to be held tightly on the larynx. This prevents anteroposterior movements of the larynx, which would alter projection. Some subjects commented that the pressure of the probe on the neck made it more difficult to change pitch at certain pitch ranges. This limited the upper pitch range of subject J. It is likely that both the supine position and the pressure of the US probe on the neck impaired the function of the muscles that could assist ventrodorsal gliding in the cricothyroid articulation (strap muscles and, e.g., geniohyoid; see Sonninen1). Therefore the subjects may have been forced to use rotation more than habitually in raising pitch or the female subjects especially may have adopted a more falsettolike singing style requiring less longitudinal stretch of the vocal folds. CONCLUSIONS The results of the present study suggest that ultrasound registration can be used in investigation of Journal of Voice, Vol. 16, No. 2, 2002
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pitch-synchronous changes in the anterior cricothyroid space. The obvious limitation of the method is that measurement points vary depending on projection. Changes in the vertical position of the larynx affect the projection. Therefore, no true values for the CT space can be obtained, and the values measured are comparable only over a limited pitch range. US registration also requires the subjects to be lying supine. This may affect voice production. The US probe has to be held tightly on the neck to prevent anteroposterior movements of the larynx. This may also interfere with the subjects’ voice control habits. Acknowledgments: The kind and patient participation of the subjects, members of the choir “Cassiopeia,” is warmly acknowledged. Thanks are also due to Mrs. Virginia Mattila, MA, for improving the manuscript.
REFERENCES 1. Sonninen A. The role of the external laryngeal muscles in length-adjustment of the vocal cords in singing. Acta Otolaryngologica. 1956;130(suppl.):1–102. 2. Berg van den Jw, Tan TS. Results of experiments with human larynges. Pract Oto-rhino-laryngologica. 1959;21:425–450. 3. Titze IR, Talkin DT. A theoretical study of the effects of various laryngeal configurations on the acoustics of phonation. J Acoust Soc Am. 1979;66(1):60–74. 4. Faaborg-Andersen K. Electromyographic investigation of intrinsic laryngeal muscles in humans. Acta Physiologica Scandinavia. 1957;41:9–148. 5. Hirano M. Phonosurgery basic and clinical investigations. Otologia (Fukuoka). 1975;Suppl. 1(21):239–440. 6. Hollien H. Vocal pitch variation related to changes in vocal fold length. J Speech Hear Res. 1960;3:150–156. 7. Sawashima M, Hirose H, Honda K, Yoshioka H, Hibi SR, Kawase N, Yamada M. Stereoendoskopic measurement of the laryngeal structure. In: Bless DM, Abbs JH, eds. Vocal Fold Physiology. San Diego, California:College-Hill Press; 1983: 264–276. 8. Nishizawa N, Sawashima M, Yonemoto K. Vocal fold length in vocal pitch change. In: Fujimura O, ed. Vocal Physiology; Voice Production, Mechanisms and Functions. New York, New York, NY: Raven Press; 1988: 75–83; Vocal fold physiology, volume 2. 9. Sonninen A, Hurme P, Laukkanen A-M. The external frame function in the control of pitch, register and singing mode: radiographic observations of a female singer. J Voice. 1999; 13(3):319–340. 10. Hirano M. Structure and vibratory behavior of the vocal folds. In: Arnold GE, Winckel F, Wyke BD, eds. Dynamic Aspects of Speech. Wien, Austria:Springer-Verlag; 1977. 11. Atkinson J. Correlation analysis of the physiological factors controlling fundamental frequency. J Acoust Soc Am. 1978;63:211–222. Journal of Voice, Vol. 16, No. 2, 2002
12. Titze I, Luschei E, Hirano M. Role of the thyroarytenoid muscle in regulation of fundamental frequency. J Voice. 1989;3(3):213–224. 13. Tanaka S, Tanabe M. Experimental study of regulation of vocal pitch. J Voice. 1989;2: 93–98. 14. Kempster GB, Larson CR, Kistler MK. Effects of electrical stimulation of cricothyroid and thyroarytenoid muscles on voice fundamental frequency. J Voice. 1988;3: 221–229. 15. Titze IR, Jiang J, Druker DG. Preliminaries to the body-cover theory of pitch control. J Voice. 1988;1:314–319. 16. Titze IR. Principles of Voice Production. Englewood Cliffs, NJ: Prentice-Hall;1994. 17. Hollien H, Moore P. Measurements of the vocal folds during changes in pitch. J Speech Hear Res. 1960;3:157–165. 18. Isshiki N. Regulatory mechanism of vocal intensity varition. J Speech Hear Res. 1965;7:17–29. 19. Hollien H. In search of vocal frequency control mechanisms. In: Bless D, Abbs J, eds. Vocal Fold Physiology. San Diego, Calif: College-Hill; 1983: 361–378. 20. Vilkman E, Takalo R, Määttä T, Laukkanen A-M, Nummenranta J, Lipponen T. Ultrasonographic measurement of cricothyroid space in speech. Proceedings of EuroSpeech '97, 5th European Conference on Speech Communication and Technology: 1997 September 22–25; Rhodes, Greece. Rhodes: European Speech Communication Association; 1997: 39–42. 21. Friedrich G, Lichtenegger R. Surgical anatomy of the larynx. J Voice. 1997;11(3):345–355. 22. Hirano M, Vennard W, Ohala J. Regulation of register, pitch, and intensity of voice. Folia Phoniatr. 1970;27:1–20. 23. Kitajima K, Tanabe M, Isshiki N. Cricothyroid distance and vocal pitch. Experimental surgical study to elevate the vocal pitch. Ann Otol. 1979;88:52–55. 24. Vilkman E, Alku P, Laukkanen A-M. Vocal-fold collision mass as a differentiator between registers in the low-pitch range. J Voice. 1995; 9(1):166–173. 25. Sonninen A, Hurme P. Vocal fold strain and vocal pitch in singing: radiographic observations of singers and nonsingers. J Voice. 1998;12:274–286. 26. Yamada H. The Strength of Biological Materials. Baltimore, Md:The Williams and Wilkins Co; 1970. 27. Williams RG, Eccles R. A new clinical measure of external laryngeal size which predicts the fundamental frequency of the larynx. Acta Otolaryngol (Stockh). 1990;110:141–148. 28. Laukkanen A-M, Mäki E, Pukander J, Anttila I. Vertical laryngeal size and the lowest tone in the evaluation of the average fundamental frequency of Finnish speakers. Logopedics Phoniatr Vocol. 1999;24(4): 170–177. 29. Müller J. Handbuch der Physiologie des Menschen. Teil I. Hölscher: Coblenz; 1837. 30. Hixon TJ. Respiratory function in speech. In: Hixon TJ & collaborators, eds. Respiratory Function in Speech and Song. Boston, Mass:College-Hill Press; 1987:1–54. 31. Sundberg J, Leanderson R, von Euler C, Knutsson E. Influence of body posture and lung volume on subglottal pressure control during singing. J Voice. 1991:5(4):283–291. 32. Vilkman E, Sonninen A, Hurme P, Körkkö P. External laryngeal frame function in voice production revisited: a review. J Voice. 1996;10(1):78–92.
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APPENDIX Pitch-synchronous changes in the CT space in each musical fifth sung by each subject. “Up” and “down” indicate change in ascending/descending fifth. Positive/negative values show an increase/a decrease in CT space. Subject A (male)
Fifth E2-B2 F2-C3 G2-D3 A2-E3 B2-F3 C3-G3 D3-A3 E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4
Up 0.28 -0.1 -0.13 -0.07 -0.2 -0.07 -0.13 -0.2 -0.15 -0.05 -0.07 -0.18 -0.22 -0.3 -0.1 -0.150 0.078
Down 0.23 0.1 0.15 0.1 0.15 0.18 0.1 0.1 0.13 0.07 0.27 0.08 0.25 0.22 0.13 0.151 0.065
G2-D3 A2-E3 B2-F3 C3-G3 D3-A3 E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4
-0.02 -0.33 -0.15 -0.25 -0.23 -0.07 -0.13 -0.07 -0.1 -0.13 -0.25 -0.25 -0.05 -0.156 0.096
0.02 0.22 0.22 0.13 0.15 0.13 0.1 0.05 0.03 0.1 0.17 0.28 0.05 0.127 0.080
E2-B2 F2-C3 G2-D3 A2-E3 B2-F3 C3-G3 D3-A3 E3-B3 F3-C4 G3-D4
-0.15 -0.28 -0.23 -0.25 -0.2 -0.15 -0.25 -0.22 -0.05 -0.13 -0.191 0.070
0.13 0.18 0.23 0.15 0.13 0.13 0.28 0.18 -0.07 0.1 0.144 0.092
Mean SD Subject B (male)
Mean SD
Subject D (male)
Mean SD
0.202
Subject E (trained male) E2-B2 F2-C3 G2-D3 A2-E3 B2-F3 C3-G3 D3-A3 E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 Mean SD 0.144
Up -0.4 -0.45 -0.35 -0.07 -0.35 -0.42 -0.28 -0.13 -0.274 0.208
Down 0.43 0.25 0.43 0.3 0.38 0.17 0.43 -0.18 0.276
0 -0.53 -0.18 -0.1 -0.1 0.05 -0.2 -0.17 0.05 -0.25 -0.15 -0.2 -0.15 -0.17 -0.150 0.120
0 0.43 0.13 0.22 0.43 0.28 0.1 0.15 0.22 0.27 0.13 0.13 0.18 0.17 0.203
-0.17 -0.25 -0.07 -0.2 -0.23 -0.22 -0.07 -0.13 -0.13 -0.07 -0.3 -0.15 -0.07 -0.13 -0.05 -0.15 -0.07 -0.145 0.075
0.2 0.15 0 0.3 0.07 0.1 0.1 0.13 0.15 0.18 0.15 0.05 0.1 0.1 0.08 0.13 0.07 0.121 0.067
Subject F (female) E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4 F4-C5 G4-D5 A4-E5 B4-F#5 C5-G5 D5-A5 E5-B5 F5-C6 G5-D6
Subject C (male)
Mean SD
Fifth C2-G2 D2-A2 E2-B2 F2-C3 G2-D3 A2-E3 B2-F3 C4-G4
Mean SD
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ANNE-MARIA LAUKKANEN ET AL Subject G (female)
Fifth D3-A3 E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4 F4-C5 G4-D5 A4-E5 B4-F#5 C5-G5 D5-A5 E5-B5
Mean SD
Up -0.07 -0.25 -0.02 -0.2 -0.25 -0.15 -0.05 -0.22 -0.1 -0.05 -0.15 -0.08 -0.05 -0.17 -0.13 -0.13
Down 0.13 0.5 0.05 0.13 0.27 0.25 0.08 0.17 0.05 0.1 0.18 0.08 0.08 0.1 0.07 0.1
-0.129
0.146
0.074
0.115
-0.1 -0.13 -0.23 -0.07 -0.13 -0.08 -0.08 -0.02 -0.08 -0.13 -0.1 -0.15 -0.108
0.05 0.1 0.1 0.05 0.02 -0.05 0.05 0 0.08 0.18 0.1 0.15 0.069
0.052
0.063
Subject H (female) E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4 F4-C5 G4-D5 A4-E5 B4-F#5 Mean SD
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Subject I (female)
Up -0.13 -0.3 -0.27 -0.25 -0.25 -0.1 -0.13 -0.07 0.08 -0.18 -0.18 -0.13 -0.1 -0.17 -0.58 -0.2
Down 0.17 0.38 0.3 0.17 0.2 0 0.08 0.07 0.05 0.22 0.13 0.2 0.12 0.13 0.3 0.4
Mean
-0.185
0.176
SD
0.140
0.125
Subject J (trained female) E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4 F4-C5
-0.13 -0.15 -0.13 -0.-05 -0.-08 -0.23 -0.13 -0.1 -0.1
0.03 0.07 0.03 0.03 0.05 0.08 0.13 0.07 0.07
Mean
-0.122
0.062
0.051
0.032
SD
Fifth C3-G3 D3-A3 E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4 F4-C5 G4-D5 A4-E5 B4-F#5 C5-G5 D5-A5
Pitch-Synchronous Changes in the Anterior Cricothyroid Space During Singing *Anne-Maria Laukkanen, †Raija Takalo, ‡Miika Arvonen, and ‡§Erkki Vilkman *Department of Speech Communication and Voice Research, University of Tampere, Tampere, Finland; †Departments of Diagnostic Radiology and ‡Otolaryngology and Phoniatrics, University of Oulu, Oulu, Finland; §Helsinki University Central Hospital, Helsinki, Finland
Summary: Pitch-synchronous changes in the anterior cricothyroid (CT) space were registered with ultrasonography (USG) for ten healthy subjects (5 males, 5 females) during the production of musical fifths throughout the whole voice range. One of the males and one of the females were trained amateur singers, the other subjects were choir singers. The average decrease in CT space per a musical fifth was 1.3–2.4 mm for the males and 1.0–1.8 mm for the females; the average decrease was smaller in the middle of the pitch range for both genders. The results suggest that (1) USG can be used for detection of pitch-synchronous changes in the CT space; (2) these changes are dependent on pitch range; and (3) more trained singers tend to have somewhat smaller changes than less trained subjects at certain frequencies. The results seem to indicate that F0 control mechanism varies according to pitch range and register, and possibly according to individual structure and vocal technique related differences. Key Words: Ultrasonography—F0 control—Singing—Register.
roarytenoid muscle (TA)10–12 and subglottic pressure in F0 control has also been studied.12–13 Contraction of TA has been found to be related either to a decrease or to an increase in F0.13–15 It has been stated that the role of TA in F0 control depends on the activity relation between TA and CT15 and on the amplitude of vibration of the vocal folds.12 Contraction of TA increases the stiffness of the muscular layer of the vocal fold. Thus, increased activity of TA raises F0 if the activity of the CT is not near its maximum and when the amplitude is large enough to involve the muscular layer of the vocal fold. This holds true for phonation at lower pitches and when the intensity of phonation is sufficiently great. When the amplitude of vibration of the vocal folds is low and the vibration concentrates mainly on the cover part, contraction of TA lowers F0, since it loosens the cover. Increased activity of the TA muscle thus tends to
INTRODUCTION Fundamental frequency (F0) can be varied by changing the vibrating mass and/or the stiffness of the vocal folds.1–3 The relationship between mass and F0 is inverse while the relationship between stiffness and F0 is direct. Stiffness can mainly be increased and the effective mass decreased by the cricothyroid (CT) muscle, which elongates the vocal folds by approximating the cricoid arch and the thyroid cartilage.4–5 There is evidence that the vocal folds lengthen as F0 is raised.1,6–9 The role of the thyAccepted for publication August 20, 2000. Address correspondence and reprint requests to Anne-Maria Laukkanen, PhD, Department of Speech Communication and Voice Research, University of Tampere, FIN-33014 Tampere, Finland. e-mail: [email protected]
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CRICOTHYROID SPACE lower F0 at high frequencies and when intensity is low. An increase in subglottic pressure may raise F0 by increasing the amplitude of vibration of the vocal folds, which in turn, increases the stiffness of the vocal fold cover.16 It has been suggested that different mechanisms may be applied at different pitch ranges11 and in different registers8,17–19 and that there may also be individual differences in the use of F0 control mechanisms.8 F0 control has mainly been studied by using x-ray and electromyographic (EMG) methods. Both methods are invasive and even risky. Noninvasive methods can also be used to some extent. For example, F0 control through activation of the cricothyroid muscle should be indicated in changes of the CT space. Those, in turn, should be seen by using ultrasound (US) examination. Vilkman et al20 studied the physiological background of sentence declination and stress production using US method. The results suggest that the method is usable for studying F0 control mechanisms. The purpose of the present study was to investigate changes in the anterior cricothyroid space as a function of changes in F0 during singing. The US method was applied. MATERIALS AND METHODS Subjects and the task Ten healthy subjects (5 males, 5 females, mean age 29.4 years, range 21–44 years) volunteered as subjects for the study. One of the males (subject E) and one of the females (subject J) were trained amateur singers with approximately 10 years and 5 years of study in classical singing. The other subjects were choir singers with an average of 8 years (range 3–19.5 years) experience but without any formal singing training, except for one, subject G, who had been studying singing for 6 years. Since, however, her singing style in these experiments did not differ from that of the other choir singers, she will be classified as an untrained choir singer in this study. The perceptual differences between the singing styles used by the choir singers and the trained singers were a more falsettolike voice quality with less marked vibrato in the choir singers, while the trained singers used a more “mixed register” type of voice quality and had a clear vibrato in their samples. The subjects sang musical fifths up and back downward (e.g. C-G-
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C) on vowel [!:] throughout their vocal range starting from the lowest sustainable tone and continuing up to the highest one. In order to keep the test duration reasonable, only those fifths were included whose starting pitches are in C major. The duration of each note sung was approximately two seconds. The task was completed twice. The subjects were lying supine during the test, which was necessary for the US registration. Ultrasonography The US examination was accomplished at the Department of Diagnostic Radiology at Oulu University Hospital by an experienced radiologist (one of the authors, RT). In the examination a real-time scanner (GE Logiq 500MD) and a 13-MHz linear transducer were used. This US transducer type has a high resolution for objects near the surface. The transducer was placed tightly against the skin anteriorly on the larynx in the midline. Figure 1 illustrates the examination procedure. The US images and the audiosignal were stored on videotape. The frame interval of the videorecorder was 40 ms. The CT space was measured in the middle of each note. The echoes caused by the calcified areas close to the anteroinferior edge of the thyroid cartilage and the anterosuperior edge of the cricoid cartilage were used as points of measurement (see Figure 2). The measurements were performed manually on a monitor screen with the aid of a pair of dividers. The monitor offered a quadruple magnification, which increases the accuracy of the measurement. The values were calibrated against the recorded scales available in the US device. For each musical fifth the optimal points of measurement, i.e., calcified areas with clearly discernible contures, were chosen. It should be noted that these points were not necessarily located exactly at the border of the cartilages. Hence the CT distance obtained does not represent the true CT space. Moreover, as the projection changes due to changes in the laryngeal position during the production of a wide pitch range, the contures of the calcified areas on the USG display change accordingly. For these reasons only changes in the CT distance for a given musical fifth can be studied using the US method. The measurements were made by an experienced radiologist (author RT). Some of the samples were Journal of Voice, Vol. 16, No. 2, 2002
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FIGURE 1. Ultrasound examination procedure.
also measured by another experimenter (author MA) to obtain interrater correlation. Frame was standardized in the measurements. The results from repeated measurements accomplished by the same examiner on two successive days did not differ significantly from each other (Student’s t test; t = 0.00, d.f. = 35, S = 1.000) and there was a perfect correlation between them (r = 1.00; P = 0.000). The results obtained by the two examiners also correlated strongly with each other (r = 0.96; P = 0.000). Figure 3 shows the correlograms. In the repeated measurements made by the same examiner the results matched perfectly in 77.7% of the cases and in 22.2% of the cases the results were within ±0.03 cm. The two examiners agreed perfectly in 11.1% of the cases, and in 55.5% of the cases the difference between their results was within ±0.03 cm. It is concluded that the measurement accuracy was sufficient.
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FIGURE 2. Longitudinal ultrasonographic scan of the anterior cricothyroid space. T = thyroid cartilage, C = cricoid cartilage. CT space measured as the distance between the points marked with an asterisk (*).
RESULTS Figures 4 and 5 show the average pitch-synchronous changes in the CT space during the production of the musical fifths both upward and downward. A comparison between trained singers and choir singers is seen in Figure 6. The pitch-synchronous changes in the CT space are given for each subject separately in the Appendix. As can be expected, CT space diminished in most cases as pitch rose, only a few exceptions were observed (see Figure 6B and Appendix). The average change in CT space per one ascending musical fifth was -0.17 cm for the males (SD = 0.12 cm) and -0.14 cm for the females (SD = 0.09 cm). Figure 4 suggests that there was a tendency for the change in CT space to be smaller in descending fifths. In Figure 5 it can be seen that this tendency was mainly true for the fe-
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A
B
FIGURE 3. Correlograms for (A) repeated measurements made by the same examiner, and for (B) measurements accomplished by two examiners.
males, while for the males the average change in CT space was in most cases larger in descending fifths. The average change in CT space was for the males the same in descending musical fifths as in ascending fifths (mean-0.17 cm, SD = 0.12 cm). For the females the average change was slightly smaller in descending fifths (mean change-0.12 cm, SD = 0.10 cm). The average difference between CT space changes in ascending and descending fifths (calculated in absolute values of the CT space change) was 0.04 cm for the females (28%) and 0.03 cm for the males (18%). The difference between the genders was nonsignificant in pitch change upward but sig-
nificant in pitch change downward (Mann-Whitney U test, U value = 63.5, ␣ = 0.01). As can be seen in Figures 4–6, the changes in CT space occurred nonlinearly and were smaller and larger at certain pitch areas. In general, smaller changes were seen in the middle of the pitch range (located mainly in the third octave for the males and in the fourth for the females) than at lower and at higher pitches (in the second and the fourth octaves for the males and in the third and the fifth octaves for the females). In the highest musical fifths the changes in CT space were, in general, small. The average change in ascending fifths at the lowest pitch-
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FIGURE 4. Average pitch-synchronous changes of the cricothyroid (CT) space (in centimeters, vertical axis) for ten subjects singing musical fifths upward and downward. A negative value shows a decrease in CT space as pitch rises. The change in CT space was positive in descending fifths but the changes are given in negative values in order to make a comparison between ascending and descending fifths easier. Numbers on the horizontal axis refer to musical fifths, 1 being the lowest produced by each subject. Number of subjects per each musical fifth: 10 for 1st–8th, 9 for 9th, 8 for 10th, 7 for 11th and 12th, 6 for 13th, 5 for 14th, 4 for 15th, 3 for 16th, and 1 for 17th.
es was -0.26 cm (SD = 0.15 cm) for the males and -0.17 cm (SD = 0.08 cm) for the females. At the middle of the pitch range the average change in CT space was -0.12 cm (SD = 0.07 cm) for the males and -0.08 cm (SD = 0.06 cm ) for the females. At the higher pitches (the highest excluded) the average change was -0.24 cm (SD = 0.08 cm) for the males and -0.17 cm (SD = 0.11 cm) for the females. The differences between the lowest and the middle pitch ranges were nonsignificant for both genders, while the middle and the highest pitch ranges differed significantly from each other (Mann-Whitney U test, for the males U value = 55.5, ␣ = 0.001, for the females U value = 63.5, ␣ = 0.001). The female choir singer, subject G, who had received singing training made an exception to the general pattern (see Appendix): For her the changes in CT space became fairly linearly smaller as pitch increased. The trained subjects (subjects E and J) showed in the middle of the range smaller changes in the CT space than the choir singers, while at the lower pitch range the largest change was seen for subject E (Figure 6). The average pitch increase related decrease in the CT space was smallest at the 3rd–4th musical fifth Journal of Voice, Vol. 16, No. 2, 2002
and at the 6th–9th musical fifth (Figure 4). For individual subjects, then, either the starting note or the ending note of these musical fifths was located at C3F#3 and D4-F#4 in the males and at D4-F#4 and C5E5 for the females (see Table 1). These pitch ranges are known as register transition areas. According to the authors’ perception the voice quality of most of the subjects changed more or less clearly toward a falsetto quality especially at the higher transition area. Friedrich and Lichtenegger21 made morphological measurements on 50 human laryngeal preparates to determine the average configurations and dimensions of cartilages and soft tissues of the larynx. Based on these measurements it can be estimated that for the males a 1-mm decrease in the CT space would bring about an increase of 1.4 mm in the length of the membraneous portion of the vocal folds, while for the females only a 0.5 mm change in length would take place. Considerable individual differences are expected, since location of the rotation center point between cricoid and thyroid cartilages naturally varies due to differences in the laryngeal geometry. Additionally, these estimations do not take into ac-
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A
B
FIGURE 5. Average pitch-synchronous change of cricothyroid (CT) space (in centimeters, vertical axis) for (A) 5 females and (B) 5 males singing musical fifths upward and downward. The change in CT space was positive in descending fifths but the changes are given in negative values in order to make a comparison between ascending and descending fifths easier. Horizontal axis: number of musical fifths, 1 being the lowest produced by each subject. Number of female subjects per musical fifths: 5 for fifths 1–9, 4 for 10–12, 3 for 13–16, and 1 for 17. Number of male subjects: 5 for fifths 1–8, 4 for 9–10, 3 for 11–13, 2 for 14, and 1 for 15.
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A
B
FIGURE 6. Average change of cricothyroid (CT) space (in centimeters, vertical axis) for one trained and four untrained females (A) and for one trained and four untrained males (B) singing musical fifths upward. Horizontal axis: number of musical fifths (1 is the lowest).
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TABLE 1. Musical Fifths with Smaller than Average PitchSynchronous Changes in the CT Space Males Subject A Subject B Subject C Subject D Subject E (trained)
A2 - E3 B2 - F3 B2 - F3 F2 - C3 A2 - E3
C3 - G3 E3 - B3 E3 - B3 C3 - G3 D3 - A3
E3 - B3 G3 - D4
Females Subject F Subject G Subject H Subject I Subject J (trained)
G3 - D4 A3 - E4 A3 - E4 A3 - E4 A3 - E4
D4 - A4 E4 - B4 E4 - B4 D4 - A4 D4 - A4
G4 - D5 A4 - E5
count the possible effect of cartilage gliding on vocal fold length. Furthermore, the effect of a change in vocal fold length on F0 is dependent on the actual stiffness of the vocal folds and subglottic pressure.12,22 Therefore only a rough estimation can be given for the relationship between a change in CT space and a change in vocal fold length. In the present study the average change in CT space per one ascending musical fifth was 1.7 mm for the males and 1.4 mm for the females. According to the estimation these changes would correspond to changes of 2.4 and 0.7 mm, respectively, in the length of the membraneous portion of the vocal folds. This, in turn, would make a change of 0.34 mm per semitone in the length of the vocal folds for the males and a change of 0.1 mm per semitone for the females. In Figure 7 changes in the CT space for subject F (female) have been translated into changes in vocal fold length and compared with the x-ray results obtained by Sonninen et al9 for pitch-synchronous changes in the distance between the anterior ossification centers of the thyroid (T) and the arytenoid (A) cartilages for one trained soprano singing in forte covered mode. This T-A distance gives approximate information of vocal fold length. Data of the present study and those of Sonninen et al bear resemblance: Pitch-synchronous changes in both the CT space and in the T-A distance were smaller in the middle of the pitch range and various dips occurred in both curves at register transition areas.
B3 - F4
G3 - D4
A4 - E5 E4 - B4
DISCUSSION Kitajima and collaborators reported that a decrease of 1 mm in the CT space of human larynx preparates (male and female larynges) brought about an increase of 0.15–0.90 semitones in pitch.23 In the present study much smaller pitch-synchronous changes in CT space were found. This discrepancy is most likely due to the higher stiffness of the vocal folds in living subjects. According to the x-ray study of Sonninen et al for 10 trained singers, the pitch-synhronous changes in the length of the vocal folds varied between 2–9.5 mm.1 When a correction for projection error is made the values are within 1.6–7.45 mm. On the basis of these values, and the pitch range sung by the subjects in Sonninen’s study, it is possible to calculate a mean change of 0.10–0.23 mm per semitone for the females and a mean change of 0.08–0.17 mm per semitone for the males. The changes observed by Nishizawa et al with stereoendoscopy were 0.7–3.5 mm per octave for the males and 1.5–2.1 mm per octave for the females (untrained singers).8 This makes a change of 0.12–0.17 mm per semitone for the females and a change of 0.06–0.29 mm per semitone for the males. The values obtained in the present study as the changes in CT space were translated into changes in vocal fold length and are reasonably within those reported by Sonninen and by Nishizawa et al. This suggests that the measurement accuracy of the US method was sufficient and that the subjects Journal of Voice, Vol. 16, No. 2, 2002
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FIGURE 7. Comparison between x-ray data on pitch-synchronous changes in thyroarytenoid distance (corresponding to vocal fold length) for one trained female soprano singing in forte covered mode and USG data on changes in cricothyroid (CT) space for one untrained female (subject F) singing musical fifths upward. Changes in CT space have been translated into changes in vocal fold length based on the measurements of Friedrich and Lichtenegger (1997). Vertical scale is in millimeters. Numbers on the horizontal axis refer to musical fifths, 1 being the lowest produced by each subject. The x-ray data were obtained from a study by Sonninen et al (1999).
accomplished F0 control mainly by rotation of the cricothyroid articulation. The average value for the males is made higher by the values of subject D. His values may be higher because he was the oldest of the choir singers (44 years) and he also had the lowest pitch range. According to the results obtained in the present study, pitch-related changes in CT space seemed to be pitch dependent. The results appear logical. In the very lowest musical fifth the pitch-synchronous decrease in CT space was smaller than that in the next musical fifth starting one tone higher. This may indicate that the role of thyroarytenoid muscle, and possibly also that of subglottic pressure in F0 regulation, is at the lowest pitch range larger than at higher pitches where F0 is mainly regulated by cricothyroid muscle. Atkinson reported (for one male subject, though) that at the lowest pitches F0 is raised through the activation of the vocalis muscle and at higher pitches the task is accomplished with the cricothyroid muscle.11 Isshiki, in turn, suggested that in falsetto register F0 is mainly regulated by subglottic pressure.18 At the very lowest pitches voice production is mainly falsettolike (characterized by incomplete glottal closure).24 The fact that smaller changes in CT space were seen in the middle pitch range might indicate deJournal of Voice, Vol. 16, No. 2, 2002
creased activity of the vocalis related to a shift from a heavier register to a lighter one (from “modal” to “middle register” or to “falsetto”). As the activity of the vocalis decreases, the vocal fold cover gets stiffer and a smaller increase in vocal fold length is needed to increase vocal fold stiffness further. This can also explain the fact that fairly small changes in CT space were seen in the highest pitches of each subject’s range. Furthermore, the changes in CT space seemed to be smallest in those musical fifths in which either the lowest or the highest tone was located at register transition areas. In the perception of the authors, the subjects also tended to decrease the intensity in those tones. In general, the results of the present study, as well as those obtained by Sonninen et al9 seem to indicate that there are various biomechanical areas or registers in human pitch range. The result that the pitch-synchronous change in CT space increased again at pitches above the middle range are also in line with the observations of Sonninen et al on changes in the T-A distance (i.e., length of the vocal folds) (see Figure 7). This might be explained as follows. The activity of both CT and TA has been found to increase simultaneously as pitch is raised.22 It is possible that at the highest pitches in a register (i.e., at pitches somewhat below a register transition) the
CRICOTHYROID SPACE activity of TA gets so strong compared to that of CT that a greater stretch of the vocal fold is needed to raise pitch further. The trained subjects showed slightly smaller changes in CT space in the middle range; this seems to suggest that trained subjects relax the vocalis more. These results are in accordance with those obtained by Sonninen et al.9,25 In trained singers and in one trained soprano singing in the “covered” mode, i.e., the typical voice production of trained singers, the pitch-synchronous increase in vocal fold length was smaller than in untrained singers and in the trained soprano’s open mode of singing, which corresponds to an untrained singer’s speechlike singing. On the other hand, the trained male singer of the present study (subject E) had a large change in CT space at the low-pitch range. This, in turn, might be explained by a strong vocalis activity. It seems plausible that at the low-pitch range this singer sang louder and with fuller modal register quality than the untrained singers. The authors’ perceptual observations support this suggestion. The female choir singer (subject G) with singing training showed the smallest CT space changes in the highest pitch range. This may reflect individual structural and/or behavioral differences. It may show that she was skilled in relaxing vocalis activity with pitch rise or that she used the purest falsetto type of voice. The observation may also be related to the fact that she had the highest soprano voice among the subjects. The change in CT space was in some cases—especially for the females—somewhat smaller during pitch change downward than when pitch was raised. For the males the change was in most cases larger in descending fifths. These findings could reflect changes in voice intensity. When intensity is lowered together with pitch, somewhat longer and thus stiffer vocal folds are needed to avoid excessive pitch drop.22 On contrast, if intensity is higher at the lowest notes of the fifths the CT space must be opened to reach as low a pitch as needed. The smaller change in CT space during pitch lowering could also be explained by the so-called hysteresis effect.26 During longitudinal stretch, a tissue, e.g., vocal fold, loses its stiffness to a certain degree. Therefore the same fundamental frequency (F0) can be obtained with longer vocal folds when pitch is shifted downward. This phenomenon seemed to be stronger in the females. This, as well as the fact that slightly smaller changes
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in CT space were measured for the females than for the males, could be explained by suggesting that the female vocal fold tissue is somewhat stiffer than that of the males. There is some evidence supporting this supposition. Various authors have come to the conclusion that differences in F0 between the sexes cannot be explained merely through differences in the laryngeal size.27,28 Nishizawa et al reported (for untrained singers) smaller pitch-synhronous changes in the vocal fold length for the females than for the males.8 Furthermore, according to the results of Müller obtained from human larynx preparates, the maximum stretch-induced change in vocal fold length was 5 mm for the males and 3 mm for the females.29 On the other hand, Sonninen and Hurme observed (for trained singers) larger pitch-synhronous length changes in the vocal folds of their female subjects compared to the male subjects.25 This discrepancy might be explained by differences in the individual and in vocal technique. A supine position may have some effect on voice production. As the direction of gravitational force changes, it alters the biomechanical conditions for the respiratory and laryngeal muscles (about respiration see, for example, Hixon and collaborators30 and Sundberg et al31; about external laryngeal frame function see Sonninen1 and Vilkman et al32). Furthermore, to obtain a clear image and to avoid projection errors, the US probe has to be held tightly on the larynx. This prevents anteroposterior movements of the larynx, which would alter projection. Some subjects commented that the pressure of the probe on the neck made it more difficult to change pitch at certain pitch ranges. This limited the upper pitch range of subject J. It is likely that both the supine position and the pressure of the US probe on the neck impaired the function of the muscles that could assist ventrodorsal gliding in the cricothyroid articulation (strap muscles and, e.g., geniohyoid; see Sonninen1). Therefore the subjects may have been forced to use rotation more than habitually in raising pitch or the female subjects especially may have adopted a more falsettolike singing style requiring less longitudinal stretch of the vocal folds. CONCLUSIONS The results of the present study suggest that ultrasound registration can be used in investigation of Journal of Voice, Vol. 16, No. 2, 2002
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pitch-synchronous changes in the anterior cricothyroid space. The obvious limitation of the method is that measurement points vary depending on projection. Changes in the vertical position of the larynx affect the projection. Therefore, no true values for the CT space can be obtained, and the values measured are comparable only over a limited pitch range. US registration also requires the subjects to be lying supine. This may affect voice production. The US probe has to be held tightly on the neck to prevent anteroposterior movements of the larynx. This may also interfere with the subjects’ voice control habits. Acknowledgments: The kind and patient participation of the subjects, members of the choir “Cassiopeia,” is warmly acknowledged. Thanks are also due to Mrs. Virginia Mattila, MA, for improving the manuscript.
REFERENCES 1. Sonninen A. The role of the external laryngeal muscles in length-adjustment of the vocal cords in singing. Acta Otolaryngologica. 1956;130(suppl.):1–102. 2. Berg van den Jw, Tan TS. Results of experiments with human larynges. Pract Oto-rhino-laryngologica. 1959;21:425–450. 3. Titze IR, Talkin DT. A theoretical study of the effects of various laryngeal configurations on the acoustics of phonation. J Acoust Soc Am. 1979;66(1):60–74. 4. Faaborg-Andersen K. Electromyographic investigation of intrinsic laryngeal muscles in humans. Acta Physiologica Scandinavia. 1957;41:9–148. 5. Hirano M. Phonosurgery basic and clinical investigations. Otologia (Fukuoka). 1975;Suppl. 1(21):239–440. 6. Hollien H. Vocal pitch variation related to changes in vocal fold length. J Speech Hear Res. 1960;3:150–156. 7. Sawashima M, Hirose H, Honda K, Yoshioka H, Hibi SR, Kawase N, Yamada M. Stereoendoskopic measurement of the laryngeal structure. In: Bless DM, Abbs JH, eds. Vocal Fold Physiology. San Diego, California:College-Hill Press; 1983: 264–276. 8. Nishizawa N, Sawashima M, Yonemoto K. Vocal fold length in vocal pitch change. In: Fujimura O, ed. Vocal Physiology; Voice Production, Mechanisms and Functions. New York, New York, NY: Raven Press; 1988: 75–83; Vocal fold physiology, volume 2. 9. Sonninen A, Hurme P, Laukkanen A-M. The external frame function in the control of pitch, register and singing mode: radiographic observations of a female singer. J Voice. 1999; 13(3):319–340. 10. Hirano M. Structure and vibratory behavior of the vocal folds. In: Arnold GE, Winckel F, Wyke BD, eds. Dynamic Aspects of Speech. Wien, Austria:Springer-Verlag; 1977. 11. Atkinson J. Correlation analysis of the physiological factors controlling fundamental frequency. J Acoust Soc Am. 1978;63:211–222. Journal of Voice, Vol. 16, No. 2, 2002
12. Titze I, Luschei E, Hirano M. Role of the thyroarytenoid muscle in regulation of fundamental frequency. J Voice. 1989;3(3):213–224. 13. Tanaka S, Tanabe M. Experimental study of regulation of vocal pitch. J Voice. 1989;2: 93–98. 14. Kempster GB, Larson CR, Kistler MK. Effects of electrical stimulation of cricothyroid and thyroarytenoid muscles on voice fundamental frequency. J Voice. 1988;3: 221–229. 15. Titze IR, Jiang J, Druker DG. Preliminaries to the body-cover theory of pitch control. J Voice. 1988;1:314–319. 16. Titze IR. Principles of Voice Production. Englewood Cliffs, NJ: Prentice-Hall;1994. 17. Hollien H, Moore P. Measurements of the vocal folds during changes in pitch. J Speech Hear Res. 1960;3:157–165. 18. Isshiki N. Regulatory mechanism of vocal intensity varition. J Speech Hear Res. 1965;7:17–29. 19. Hollien H. In search of vocal frequency control mechanisms. In: Bless D, Abbs J, eds. Vocal Fold Physiology. San Diego, Calif: College-Hill; 1983: 361–378. 20. Vilkman E, Takalo R, Määttä T, Laukkanen A-M, Nummenranta J, Lipponen T. Ultrasonographic measurement of cricothyroid space in speech. Proceedings of EuroSpeech '97, 5th European Conference on Speech Communication and Technology: 1997 September 22–25; Rhodes, Greece. Rhodes: European Speech Communication Association; 1997: 39–42. 21. Friedrich G, Lichtenegger R. Surgical anatomy of the larynx. J Voice. 1997;11(3):345–355. 22. Hirano M, Vennard W, Ohala J. Regulation of register, pitch, and intensity of voice. Folia Phoniatr. 1970;27:1–20. 23. Kitajima K, Tanabe M, Isshiki N. Cricothyroid distance and vocal pitch. Experimental surgical study to elevate the vocal pitch. Ann Otol. 1979;88:52–55. 24. Vilkman E, Alku P, Laukkanen A-M. Vocal-fold collision mass as a differentiator between registers in the low-pitch range. J Voice. 1995; 9(1):166–173. 25. Sonninen A, Hurme P. Vocal fold strain and vocal pitch in singing: radiographic observations of singers and nonsingers. J Voice. 1998;12:274–286. 26. Yamada H. The Strength of Biological Materials. Baltimore, Md:The Williams and Wilkins Co; 1970. 27. Williams RG, Eccles R. A new clinical measure of external laryngeal size which predicts the fundamental frequency of the larynx. Acta Otolaryngol (Stockh). 1990;110:141–148. 28. Laukkanen A-M, Mäki E, Pukander J, Anttila I. Vertical laryngeal size and the lowest tone in the evaluation of the average fundamental frequency of Finnish speakers. Logopedics Phoniatr Vocol. 1999;24(4): 170–177. 29. Müller J. Handbuch der Physiologie des Menschen. Teil I. Hölscher: Coblenz; 1837. 30. Hixon TJ. Respiratory function in speech. In: Hixon TJ & collaborators, eds. Respiratory Function in Speech and Song. Boston, Mass:College-Hill Press; 1987:1–54. 31. Sundberg J, Leanderson R, von Euler C, Knutsson E. Influence of body posture and lung volume on subglottal pressure control during singing. J Voice. 1991:5(4):283–291. 32. Vilkman E, Sonninen A, Hurme P, Körkkö P. External laryngeal frame function in voice production revisited: a review. J Voice. 1996;10(1):78–92.
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APPENDIX Pitch-synchronous changes in the CT space in each musical fifth sung by each subject. “Up” and “down” indicate change in ascending/descending fifth. Positive/negative values show an increase/a decrease in CT space. Subject A (male)
Fifth E2-B2 F2-C3 G2-D3 A2-E3 B2-F3 C3-G3 D3-A3 E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4
Up 0.28 -0.1 -0.13 -0.07 -0.2 -0.07 -0.13 -0.2 -0.15 -0.05 -0.07 -0.18 -0.22 -0.3 -0.1 -0.150 0.078
Down 0.23 0.1 0.15 0.1 0.15 0.18 0.1 0.1 0.13 0.07 0.27 0.08 0.25 0.22 0.13 0.151 0.065
G2-D3 A2-E3 B2-F3 C3-G3 D3-A3 E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4
-0.02 -0.33 -0.15 -0.25 -0.23 -0.07 -0.13 -0.07 -0.1 -0.13 -0.25 -0.25 -0.05 -0.156 0.096
0.02 0.22 0.22 0.13 0.15 0.13 0.1 0.05 0.03 0.1 0.17 0.28 0.05 0.127 0.080
E2-B2 F2-C3 G2-D3 A2-E3 B2-F3 C3-G3 D3-A3 E3-B3 F3-C4 G3-D4
-0.15 -0.28 -0.23 -0.25 -0.2 -0.15 -0.25 -0.22 -0.05 -0.13 -0.191 0.070
0.13 0.18 0.23 0.15 0.13 0.13 0.28 0.18 -0.07 0.1 0.144 0.092
Mean SD Subject B (male)
Mean SD
Subject D (male)
Mean SD
0.202
Subject E (trained male) E2-B2 F2-C3 G2-D3 A2-E3 B2-F3 C3-G3 D3-A3 E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 Mean SD 0.144
Up -0.4 -0.45 -0.35 -0.07 -0.35 -0.42 -0.28 -0.13 -0.274 0.208
Down 0.43 0.25 0.43 0.3 0.38 0.17 0.43 -0.18 0.276
0 -0.53 -0.18 -0.1 -0.1 0.05 -0.2 -0.17 0.05 -0.25 -0.15 -0.2 -0.15 -0.17 -0.150 0.120
0 0.43 0.13 0.22 0.43 0.28 0.1 0.15 0.22 0.27 0.13 0.13 0.18 0.17 0.203
-0.17 -0.25 -0.07 -0.2 -0.23 -0.22 -0.07 -0.13 -0.13 -0.07 -0.3 -0.15 -0.07 -0.13 -0.05 -0.15 -0.07 -0.145 0.075
0.2 0.15 0 0.3 0.07 0.1 0.1 0.13 0.15 0.18 0.15 0.05 0.1 0.1 0.08 0.13 0.07 0.121 0.067
Subject F (female) E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4 F4-C5 G4-D5 A4-E5 B4-F#5 C5-G5 D5-A5 E5-B5 F5-C6 G5-D6
Subject C (male)
Mean SD
Fifth C2-G2 D2-A2 E2-B2 F2-C3 G2-D3 A2-E3 B2-F3 C4-G4
Mean SD
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ANNE-MARIA LAUKKANEN ET AL Subject G (female)
Fifth D3-A3 E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4 F4-C5 G4-D5 A4-E5 B4-F#5 C5-G5 D5-A5 E5-B5
Mean SD
Up -0.07 -0.25 -0.02 -0.2 -0.25 -0.15 -0.05 -0.22 -0.1 -0.05 -0.15 -0.08 -0.05 -0.17 -0.13 -0.13
Down 0.13 0.5 0.05 0.13 0.27 0.25 0.08 0.17 0.05 0.1 0.18 0.08 0.08 0.1 0.07 0.1
-0.129
0.146
0.074
0.115
-0.1 -0.13 -0.23 -0.07 -0.13 -0.08 -0.08 -0.02 -0.08 -0.13 -0.1 -0.15 -0.108
0.05 0.1 0.1 0.05 0.02 -0.05 0.05 0 0.08 0.18 0.1 0.15 0.069
0.052
0.063
Subject H (female) E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4 F4-C5 G4-D5 A4-E5 B4-F#5 Mean SD
Journal of Voice, Vol. 16, No. 2, 2002
Subject I (female)
Up -0.13 -0.3 -0.27 -0.25 -0.25 -0.1 -0.13 -0.07 0.08 -0.18 -0.18 -0.13 -0.1 -0.17 -0.58 -0.2
Down 0.17 0.38 0.3 0.17 0.2 0 0.08 0.07 0.05 0.22 0.13 0.2 0.12 0.13 0.3 0.4
Mean
-0.185
0.176
SD
0.140
0.125
Subject J (trained female) E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4 F4-C5
-0.13 -0.15 -0.13 -0.-05 -0.-08 -0.23 -0.13 -0.1 -0.1
0.03 0.07 0.03 0.03 0.05 0.08 0.13 0.07 0.07
Mean
-0.122
0.062
0.051
0.032
SD
Fifth C3-G3 D3-A3 E3-B3 F3-C4 G3-D4 A3-E4 B3-F#4 C4-G4 D4-A4 E4-B4 F4-C5 G4-D5 A4-E5 B4-F#5 C5-G5 D5-A5